Integrative and Comparative Biology, volume 50, number 2, pp. 237–250
doi:10.1093/icb/icq060
SYMPOSIUM
Ephemeral Bio-engineers or Reef-building Polychaetes: How Stable
are Aggregations of the Tube Worm Lanice conchilega (Pallas, 1766)?
Ruth Callaway,1,* Nicolas Desroy,† Stanislas F. Dubois,‡ Jérôme Fournier,§ Matthew Frost,ô
Laurent Godet,§ Vicki J. Hendrick|| and Marijn Rabaut#
*Deptartment for Pure and Applied Ecology, Wallace Building, Swansea University, Singleton Park, Swansea, SA2 8PP,
UK; †CRESCO IFREMER, 38 Rue du Port Blanc, 35800 Dinard, France; ‡Laboratoire DYNECO/Ecologie Benthique,
IFREMER-Technopole de Brest-Iroise, B.P. 70 – 29280 Plouzané, France; §CNRS UMR 7208, CRESCO MNHN, 38,
Rue du Port Blanc, 3500 Dinard, France; ôMarine Biological Association of the United Kingdom, The Laboratory,
Citadel Hill, Plymouth, PL1 2PB, UK; ||Scottish Association for Marine Science, Scottish Marine Institute, Oban Argyll,
PA37 1QA, Scotland, UK; #Ghent University, Biology Department, Marine Biology Section, Sterre Campus,
Krijgslaan 281-S8, B-9000 Ghent, Belgium
From the symposium ‘‘Marine Ecosystem Engineers in a Changing World: Establishing Links across Systems’’ presented
at the annual meeting of the Society for Integrative and Comparative Biology, January 3–7, 2010, at Seattle, Washington.
1
E-mail: [email protected]
Synopsis Dense aggregations of tube-worms can stabilize sediments and generate oases for benthic communities that are
different and often more diverse and abundant than those of the surroundings. If these features are to qualify as biogenic
reefs under nature-conservation legislation such as the EC Habitats Directive, a level of stability and longevity is desirable
aside from physical and biological attributes. Lanice conchilega (Pallas, 1766) is widely distributed around the European
coast and aggregations of this tube-dwelling polychaete are known to have a positive effect on the biodiversity of
associated species in inter- and sub-tidal areas. This increases the value of L. conchilega-rich habitats for higher trophic
levels such as birds and fish. However, L. conchilega is currently not recognized as a reef builder primarily due to
uncertainty about the stability of their aggregations. We carried out three studies on different spatial and temporal
scales to explore a number of properties relating to stability: (1) Individual aggregations of L. conchilega of 1 m2
were monitored for up to 1 year, (2) records of L. conchilega from a 258-ha area over a 35-year period were analyzed,
(3) the recovery of a population of L. conchilega subjected to disturbances by cultivation of Manila clams (Ruditapes
philippinarum) was followed over 3 years. The studies provided evidence about the longevity of L. conchilega aggregations,
their resistance to disturbance, their resilience in recovering from negative impact and their large-scale persistence. The
results showed that populations of L. conchilega were prone to considerable fluctuation and the stability of aggregations
depended on environmental factors and on recruitment. The tube-worms proved to be susceptible to disturbance by
cultivation of Manila clams but demonstrated the potential to recover from that impact. The long-term monitoring of a
large L. conchilega population in the Bay of Mont Saint Michel (France) indicated that aggregations can persist over many
decades with a constant, densely populated core area and an expanding and contracting more thinly populated fringe
zone. The stability of aggregations of L. conchilega and the structures they form do not unequivocally fit the currently
accepted definition of a reef. However, given L. conchilega’s accepted reef-like potential to influence diversity and
abundance in benthic communities, we suggest clarifying and expanding the definition of reefs so that species with
records of significant persistence in particular areas and which otherwise meet expectations of reefs are included within
the definition.
Introduction
Tube-building worms such as Sabellaria alveolata,
Serpula vermicularis, or Ficopomatus enigmaticus can
develop dense aggregations of intertwined tubes
giving rise to large structures that are considered to
be biogenic reefs (Fornos et al. 1997; Dubois et al.
2002; Poloczanska et al. 2004). Such reefs induce the
stabilization of sediments (Murray et al. 2002) while
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238
the tubes of the organisms themselves provide complex structural habitats for attachment of sessile
organisms (Dubois et al. 2006) and refuge or a
food source for vagile vertebrates and invertebrates
(Bruschetti et al. 2009). Reef structures can therefore
be seen as biodiversity hotspots where species diversity deeply contrasts with that of surrounding sediments (Dubois et al. 2002). Due to their high-density
polychaete reefs can also be seen as large biological
filters and they play a significant role in trophic webs
(Bruschetti et al. 2008; Dubois et al. 2009). Biogenic
reefs are consequently of high importance to the
ecological functioning of the habitats and areas in
which they are found and it is for this reason that
reefs are of particular interest to nature conservation.
As a result, the conservation status of biogenic reefs
is recognized by legislative regulations such as the EC
Habitats Directive (Council Directive EEC/92/43 on
the Conservation of Natural Habitats and of Wild
Fauna and Flora), which lists reefs as a marine habitat to be protected by the designation of Special
Areas of Conservation (European Commission DG
Environment 2007). A number of biogenic reef
types are also listed as threatened or declining by
OSPAR (Ospar Convention for the Protection of
the Marine Environment of the north–east
Atlantic.) (Ospar Commission 2006).
According to the EC Habitats Directive ‘‘Reefs can
be either biogenic concretions or of geogenic origin.
They are hard compact substrata on solid and soft
bottoms, which arise from the sea floor in the sublittoral and littoral zone. Reefs may support a zonation of benthic communities of algae and animal
species as well as concretions and corollogenic concretions’’ (Council Directive EEC/92/43 on the
Conservation of Natural Habitats and of Wild
Fauna and Flora). Biogenic concretions are further
defined as: concretion, encrustation, corallogenic
concretions, and bivalve mussel beds originating
from dead or living animals, i.e. biogenic hard bottoms which supply habitats for epibiotic species. For
the North Atlantic region, polychaetes such as
Sabellaria spinulosa, S. alveolata, and S. vermicularis,
the bivalves Modiolus modiolus and Mytilus sp. as
well as cold-water corals are specified as examples
of characteristic reef forming species.
More detailed interpretations of this definition
suggest that reefs should meet certain physical, biological, and temporal attributes (Holt et al. 1998;
Hendrick and Foster-Smith 2006), with an expectation that they should be discrete, elevated structures
covering a substantial area. Reef-builders should bind
sediment and replace existing substratum with a new
R. Callaway et al.
one and be colonized by a different benthic community than that occurring in the surrounding area.
In addition, reefs are also considered to be stable
and to have a proven longevity since it is expected
that a long-lived, stable biogenic concretion would
have greater value in respect to conservation than
would an otherwise comparable habitat of an ephemeral nature. Nevertheless, it is generally accepted that
many reef-building organisms are to a certain degree
ephemeral. Some beds of Mytilus edulis in the
Wadden Sea, for example, may occupy the same
sites for decades while others are short-lived
(Herlyn et al. 2008). Similarly, a broad-scale UKwide study showed that S. alveolata aggregations
can appear and disappear at sites at a range of
time scales from inter-annual to multi-decadal
(Frost et al. 2004). In the case of S. spinulosa, longevity has been used as justification by the UK
Biodiversity Group to differentiate between encrusting colonies of the species and the more upright
morphology of the reefs. The group noted
that crusts are not considered to constitute true
S. spinulosa reef habitats because of their ephemeral
nature, stating that they do not provide a stable
biogenic habitat enabling associated species to
become established in areas where they otherwise
would be absent (UK Biodiversity Group 1999).
Despite this, S. spinulosa, S. alveolata, and M. edulis
are all specifically recognized as biogenic reef
builders under the EC Habitats Directive.
This article focuses on the stability and longevity
of aggregations of the tube-building sand mason
worm L. conchilega. It is a terebellid polychaete
(Figs. 1 and 2) that can form aggregations in coastal
areas to a depth of 100 m, reaching densities of
several thousand individuals per meter square
(Hertweck 1995; Ropert and Dauvin 2000). It is an
amphiboreal species found on all coasts of Europe
and in both the Atlantic and the Pacific, but it is
absent from arctic waters (Holthe 1978). Their tubes
have a diameter of 0.5 cm and are up to 65-cm
long (Ziegelmeier 1952), consisting of sand particles
attached to an inner thin organic layer. The anterior
end of the tube protrudes above the surface of the
sediment by 1–4 cm and it has a fringe made of
single-strand ‘‘sand hair’’. Lanice conchilega can
switch between deposit feeding and suspension feeding (Buhr 1976). The larvae are planktonic and were
termed ‘‘aulophore’’ by Kessler (1963) because of
their transparent tube that is used as a floating
device.
In recent years, considerable efforts were made to
assess the value of dense aggregations of L. conchilega
for the inhabited environments. Once densities reach
Stability of tube-worm aggregations
239
Fig. 1 Location of study sites (filled circle) inhabited by L. conchilega. Study A: ‘‘Small scale stability of L. conchilega’’ was carried out at
sites in the German Wadden Sea and in Wales, UK (1). Study B: ‘‘Long-term stability’’ was carried out in the Bay of Mont Saint Michel
(BMSM), France (2). Study C: ‘‘The recovery of L. conchilega aggregations impacted by clam cultivation’’ was carried out in the
Normand-Breton Gulf (France) (2).
about 500 individuals meter square the tubes start
consolidating the sediment and create a moundand-trough topography (Rabaut et al. 2009).
Aggregations of tubes were shown to provide
niches for a different and generally more speciesrich and abundant faunal community than the adjacent tube-free sands in both inter- and sub-tidal
areas (Rabaut et al. 2007; Van Hoey et al. 2008).
This has a positive knock-on effect for birds and
fish (Godet et al. 2008; Rabaut et al. 2010).
Despite demonstrating many features considered
characteristic of biogenic reefs, L. conchilega aggregations were specifically excluded from a review of
reefs for conservation management by Holt et al.
(1998) due to their assumed instability. Since then,
aggregations of L. conchilega have been described as
ephemeral in the Wadden Sea after a population was
eradicated by low winter temperatures (Zühlke
2001), and Rabaut et al. (2009) discussed the lack
of long-term data to estimate their temporal characteristics, emphasizing the lack of knowledge about
their stability and longevity.
The aim of this article is to address the gap in
knowledge regarding the longevity of aggregations
of L. conchilega. We hypothesized that the stability
of L. conchilega aggregations differs between different
spatial and temporal scales, i.e., that individual
aggregations on a scale of square meters may be
short lived and ephemeral, but that the presence of
the tube-worm is more persistent on larger spatial
and temporal scales. We further hypothesized that
aggregations of L. conchilega have the potential to
recover from disturbance. We analyzed our studies
in view of particular stability properties adapted
from Grimm et al. (1999).
Constancy: the duration of a system to remain
essentially unchanged, i.e., how long do aggregations
of L. conchilega exist without interruption? How old
are individual aggregations?
Resistance: the capability of a system to remain
unchanged despite the presence of disturbances
which could potentially change the system, i.e.,
what is the capacity for L. conchilega aggregations
to remain unaffected in the presence of natural or
anthropogenic disturbances such the harvesting of
bivalves?
Resilience and Elasticity: this refers to the property
to return to a reference state after a temporary disturbance and to the speed of recovery. Resilience is
also defined as the capacity of a system to renew and
sustain specified conditions or processes in spite of
exogenous disturbances or changes in driving forces
240
R. Callaway et al.
Fig. 2 Small-scale distribution of L. conchilega within fixed 0.5 1.5 m plots at three differently exposed sites. Densities of L. conchilega
tubes in 100-cm2 grid cells are shown. (A) Site 1 was in the Wadden Sea (Germany) and monitored four times over 1 year, (B) Site 2
was in Swansea Bay (Wales, UK) and monitored over 7 months. (C) Site 3 was in Rhossili Bay (Wales, UK) monitored over 3 months.
The cosine similarity index between consecutive monitoring dates is given. One plot per site is shown. Images on the left show a single
L. conchilega tube (top) and L. conchilega aggregations with a schematic monitoring plot (bottom).
(Carpenter and Folke 2006), i.e., are aggregations of
L. conchilega returning to their original state after
being disturbed? How quickly do aggregations
recover (elasticity)?
Persistence: the property of a system to exist
over long periods of time, where the ecological
system and disturbances affecting the system are
seen as a unit. In contrast to constancy, which
is defined as the continuous presence of a feature,
persistence allows for the intermittent absence
of the relevant population, community or other feature, if it recovers at some point, i.e., do aggregations
of L. conchilega exist over long periods of time
with phases of continuous presence alternating
241
Stability of tube-worm aggregations
with phases of disturbance, or even absence, and
recovery?
Three studies on different spatial and temporal
scales were carried out to investigate these properties
of stability.
(i) Individual aggregations of L. conchilega of
1 m2 were monitored for up to 1 year.
(ii) Records for L. conchilega on a 258-ha area over
a 35-year period were analyzed.
(iii) The recovery of a population of L. conchilega
between disturbances by cultivation of Manila
clams (R. philippinarum) was followed over
3 years.
Material and methods
Small- and large-scale studies on the stability of
L. conchilega aggregations were carried out at intertidal sites in France, Germany, and the United
Kingdom (Fig. 1).
Small-scale stability of L. conchilega
The constancy of individual aggregations of
L. conchilega was studied at three sites subjected to
different degrees of exposure (Fig. 1).
Site 1 (sheltered): ‘‘Dornumer Nacken’’, a
sheltered sandflat in the German Wadden Sea
(538 41.73’N, 078 28.30’ E, from July 1994 to
July 1995). The tidal range was 3 m and the
area was protected from major hydrodynamic
impacts by the backbarrier Island of Baltrum.
Site 2 (moderately exposed): Swansea Bay, a
15-km wide inlet east of the Gower Peninsula,
South Wales, UK (518 35.21’ N, 038 58.98’ E,
from April to October 1998). Tidal currents were
strong due to a tidal range of 11 m, but the bay
was sheltered from major exposure to waves by the
headland ‘‘Mumbles Head’’.
Site 3 (exposed): Rhossili Bay, a sandy beach at the
western tip of the Gower Peninsula, South Wales,
UK (518 34.08’ N, 048 17.88’ W, from April to
June 1998). There the tidal range was 11 m
and the area was exposed to high-energy waves
generated in the Bristol Channel.
In order to evaluate the stability of individual
aggregations, plots of 0.75 m2 were marked at the
sites (Site 1, n ¼ 3; Site 2, n ¼ 2; Site 3, n ¼ 2).
Because of the low number of replicates this study
is limited. It provides broad insight into the subject
and we were cautious not to over-interpret the data
and only report unambiguous trends. Tube tops were
counted in 100-cm2 cells arranged in a 15 5 grid.
The number of tube-tops is highly correlated with
the number of individuals burrowed in the sediment
(Ropert and Dauvin 2000; Strasser and Pieloth 2001;
Zühlke 2001; Callaway 2003; Bendell-Young 2006)
and the error associated does not exceed 3%
(Ropert 1999). Adult and juvenile tube-worms were
distinguished by size. Tubes 5 mm in diameter
were classed as adults, tubes 1–2 mm in diameter
as juveniles. Each marked plot was monitored and
counted repeatedly over time. Site 1 was monitored
for 1 year and Sites 2 and 3 for 6 and 3 months,
respectively, due to premature termination of the
studies by storms washing away the plot markers.
The similarity of the distribution pattern of
L. conchilega between dates was estimated to determine whether aggregations remained at the same
place over time. The relative position of aggregations
and tube-free areas and their constancy was analyzed
by calculating the cosine similarity between abundances, A, of tubes tops at dates j and k (Ludwig
and Rynolds 1988; Blome et al. 1999), with n being
the number of cells.
n P
j
Ai Aki
i¼1
c cosjk ¼ sffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
n 2 P
n P
2
j
Ai
Aki
i¼1
i¼1
The similarity between two dates was high if the
relative abundance in the single cells was similar; it is
1 if the relative abundance (relative frequency) in all
the single cells was exactly equal, and it is 0 if the
distribution of L. conchilega was inverse between
dates.
In order to check whether tubes were randomly
distributed or significantly clustered, the index of
dispersion was calculated. The index is based on
the variance-to-mean ratio and chi-square statistic
was used to test for significant difference from a
theoretical Poisson distribution (Ludwig and
Reynolds 1988; Blome et al. 1999).
Stability of an aggregation of L. conchilega over
35 years in the Bay of Mont Saint Michel (BMSM)
The presence of L. conchilega colonizing a 258-ha
area was studied in the BMSM, France (48839.33’
N, 01837.39’ O) (Fig. 1). The beds of L. conchilega
were mapped on a Geographical Information System
(GIS) (Arcview 3.1) via photo-interpretation processing for 1973, 1982, 2002 and 2008 [L. conchilega
aggregations can be detected on aerial photographs
(1:10000 scale) from 250 ind m2, Laurent Godet
personal observation]. Each date corresponds to a
242
specific map and to a specific layer in the GIS. In
addition, the spatial distribution of L. conchilega densities was examined within the area in 2005, 2006,
2007 and 2008. Densities were estimated by taking
numerical pictures of three 0.25-m2 random quadrats
in the middle of 362 regularly distributed stations
(cells of 1 ha) covering the area. The number of
intact tube-tops was counted on the pictures. Data
from each year were superimposed as different layers
with the GIS to distinguish between seven levels of
stability (Fig. 3), resulting in a ‘‘stability map’’.
In order to compare densities with the stability of
the aggregation two steps were taken:
(a) The ‘‘stability map’’ was divided into 1-ha cells
corresponding to the sample design used to
assess the distribution, and for each cell a ‘‘stability
index’’ was computed (stability index ¼ percentage
of the cell covering a stability level (levels 1–7)
level number).
(b) For every cell, the mean and standard deviation of
densities (2005–2008) were correlated with the
‘‘stability index’’ (R software).
Recovery of aggregations of L. conchilega impacted
by cultivation of clams
In the Chausey archipelago, Normand-Breton Gulf,
France (48853.26’ N, 01849.17’ O) (Fig. 1), Toupoint
et al. (2008) demonstrated that cultivation of Manila
clams (R. philippinarum) had strong effects on
L. conchilega aggregations. Beyond this snap-shot
study, we monitored the densities of L. conchilega
in the same aggregation over 3 years and tested the
potential resistance and resilience of the aggregation
to this shellfish culture.
Clam cultivation is a highly mechanized activity in
this region using tractor-driven machines during a
production cycle which consists of three steps:
(1) spat seeding; (2) no activities for 2 years to let
the bivalves grow; and (3) harvesting (Toupoint
et al. 2008). The highest impacts on L. conchilega
correspond with steps (1) and (3). We tested the
potential for recovery of L. conchilega over a 3-year
period (2005–2007), expecting re-colonization of
L. conchilega during step (2).
Each spring from 2005 to 2007, the spatial distribution of L. conchilega was examined in 1.28-ha plots
(80 160 m) located in three areas of clam cultivation (A, B, and C) and, as a reference, in one area in
which clams were not cultivated. The cultivation
areas differed in terms of the timing of mechanically
seeding and harvesting spat. Area A was seeded
before spring 2005, area B was harvested and reseeded between spring 2006 and spring 2007 and
R. Callaway et al.
area C was harvested and re-seeded between spring
2005 and spring 2006 (Fig. 4).
Each plot was divided into 50 cells (cell ¼ 256 m2),
and in each cell, three 0.25-m2 randomly placed
quadrates were photographed. The number of tubetops with sand-fringes was counted as a proxy for
the number of individuals burrowed in the sediment.
The spatial distributions of L. conchilega were
plotted by interpolating mean abundances and the
linear kriging method using SurferTM software.
Differences between mean densities of L. conchilega
from year-to-year were tested with nonparametric
Kruskall–Wallis tests (KW) (R software). The
assumptions of homoscedasticity were tested by
Bartlett tests. In the case of significant global analysis, post hoc comparisons were performed through
Tukey HSD tests or multiple comparison tests after
KW (R software, package pgirmess).
Results
Small-scale and short-term stability of L. conchilega
Exposure of the sites and the success of recruitment
of juveniles determined the similarity or dissimilarity
of small-scale distributional patterns over time.
At the most sheltered site, Site 1 in the Wadden
Sea, L. conchilega aggregations within the three
0.75-m2 plots remained generally at the same place
over the 1-year period. The similarity index, indicating the relative spatial similarity between distributional patterns over time, was higher at Site 1 than
at the more exposed Sites 2 and 3 in South Wales
(Fig. 2). Lowest similarities, i.e., the least consistent
aggregations, were found at the most exposed Site 3
(Rhossili Bay).
A striking difference between the sites was the
recruitment success of juvenile L. conchilega. At the
sheltered Site 1 no recruitment of juvenile L. conchilega occurred. At Sites 2 and 3, large numbers of
juveniles settled in dense clusters between April and
June, which changed the distribution pattern from
random to significantly clustered (Index of dispersion, chi-square test, n ¼ 75, P50.01). Many of the
juveniles were lost shortly after the initial settlement
and the degree of clustering decreased, particularly at
Site 3 (Fig. 2).
The varying recruitment success had an impact on
densities. Without recruitment of juveniles the density of L. conchilega at Site 1 decreased from
10.4 10.8 to 6.5 5.2 individuals 100 cm2
(n ¼ 225) over 1 year. At the moderately exposed
Site 2, densities increased from 2.6 2.0 to
4.2 3.1 individuals 100 cm2 (n ¼ 150) from April
to October, peaking at 21 18.3 in May when
Stability of tube-worm aggregations
243
Fig. 3 Persistence and density of an aggregation of L. conchilega in the B MSM, France, from 1973 to 2008. Levels of stability were based
on photo-interpretation of distribution maps of L. conchilega. In the table ‘‘X’’ correspond to the presence of an aggregation of
L. conchilega as detected via the photo-interpretation process.
244
R. Callaway et al.
Fig. 4 Recolonization of L. conchilega in an area of Manila clam cultivation in the Chausey archipelago, Normand-Breton Gulf, France.
The timing of seeding of spats and harvesting of clams is indicated. Three 80 160-m plots were monitored (Studies A–C) as was one
reference plot (natural aggregation).
juveniles had just settled. At the most exposed Site 3,
densities increased from 0.4 0.8 to 1.7 2.7 individuals 100 cm2 (n ¼ 150) from April to June.
Stability of an aggregation of L. conchilega over
35 years in the BMSM
At maximum spread the L. conchilega population
covered an area of 258 ha. The most persistent
parts of the aggregation, present at all monitoring
dates, covered 21 ha, i.e., 8% of the area of maximum spread. Fifty percent of the L. conchilega inhabited area showed medium levels of stability (2–6),
whilst 41% was categorized as unstable with a stability level of 1. The most stable area was located at the
core of the bed with stability decreasing with distance from the core (Fig. 3).
Densities and persistence of L. conchilega over time
were positively correlated; the higher their densities
245
Stability of tube-worm aggregations
the more persistent was their presence (linear model,
adjusted R2: 0.2869, F-statistic: 118.1, 290 df,
P50.01). Variance of densities and persistence were
also positively correlated (linear model, adjusted R2:
0.1926, F-statistic: 70.42, 290 df, P50.01).
The recovery of aggregations of L. conchilega
impacted by cultivation of clams
During the 2-year period between disturbances by
seeding and harvesting of Manila clams, L. conchilega
significantly re-colonized areas A and C (KW,
P50.01) whereas no significant differences were
observed in area B (KW, P ¼ 0.22) (Fig. 4). The recolonization pattern at the beginning of this period
indicated that re-colonization took place from the
periphery of the clam areas. However, L. conchilega
did not reach densities as high as in the reference
area in any of the three areas of clam cultivation.
Discussion
Our small- and large-scale studies showed that the
stability of L. conchilega aggregations depended considerably on environmental factors and recruitment.
The small-scale study, for instance, indicated that the
stability of aggregations was determined by exposure
of the site and by success of recruitment. In the
larger study plots of the Chausey archipelago, L. conchilega was found to be susceptible to disturbance by
Manila clam cultivation but had the potential to
recover to a degree, while the long-term monitoring
of the L. conchilega population in the BMSM indicated that under suitable conditions aggregations can
persist over many decades.
Lanice conchilega is widely distributed and appears
to tolerate a range of levels of exposure, although
dense aggregations seem to form under more sheltered conditions (Hertweck, 1995). Our studies suggest that the level of exposure is also negatively
correlated with the constancy of tube aggregations.
This is likely to be a reflection of the ease of recruitment since juveniles of the tube-worm in particular
are likely to be affected by severe movements of
sediment (Zühlke and Reise, 1994).
Larval recruitment is paramount for the renewal
of L. conchilega aggregations. Similar to other colonyforming invertebrates, juveniles of L. conchilega settle
in close vicinity to their conspecific adults and it
appears that hydrodynamic changes generated by
biogenic mounds induce the pelagic larvae to settle
on existing aggregations (Callaway 2003, Rabaut
et al. 2009). Our studies showed that recruitment
can fail over an entire year, which is most likely
due to unfavourable environmental conditions with
high mortality rates of the planktonic larvae
or unsuitable conditions for the settling of juveniles.
High year-to-year variation in recruitment success is
known from other tube-dwellers such as S. alveolata
where episodic events of massive settlement alternate
with the lack of larval supply (Wilson, 1971, Dubois
et al., 2007). It is possible that Sabellaria reefs are less
susceptible to the lack of rejuvenation for a few years
due to their more durable tubes and their longevity.
They reach on average an age of 3–4 years (Caline
et al. 1992), while the life span of L. conchilega is
only 1–2 years (Beukema et al. 1978). Our study
showed that a year without juvenile recruitment
resulted in decreasing abundance of L. conchilega,
but the population did not collapse. This suggests
that aggregations of L. conchilega can survive years
of failed recruitment, in particular when overall densities of the tube-worm are high. However, given
their limited life span, recurrent failure of recruitment for 2 or 3 years should lead to the population’s
demise.
Stability properties
The three studies gave insight into various stability
properties.
Constancy
Our studies showed that individual aggregations may
be either, short-lived or constant over long periods
of time. Aggregations demonstrated the potential to
remain constant for at least 1 year, substantiating
reports of similar time-spans for L. conchilega
mounds (Carey 1987). However, on a broader spatial
scale, L. conchilega have remained continuously present in specific areas for much longer. In the B
MSM, areas with high densities of L. conchilega
remained constant for the past two decades (Godet
et al. 2008).
Resistance
Our results suggest that despite their ability to
rapidly rebuild and repair the tube (Nicolaidou
2003), L. conchilega does not necessarily resist sediment disturbance. The direct physical disturbance
caused by seeding and harvesting of Manila clams
negatively affected the presence of L. conchilega,
with the most damaging practice being the scraping
of the surface sediment layer during harvesting
(Toupoint et al. 2008). The cultivation of clams
not only has drastic effects on the total abundance
of L. conchilega, but also modifies their spatial pattern and alters the associated benthic assemblage
(Toupoint et al. 2008). The resulting alternation of
habitat has knock-on effects for higher trophic levels
246
with the area losing its attractiveness as a feeding
ground for Oyster catchers (Haematopus ostralegus)
(Godet et al. 2009). In sub-litoral regions also, suction dredging of Manila clams was found to have an
equally negative effect on numbers of L. conchilega,
although after 7 months the initially severe impact
was hardly detectable (Kaiser et al. 1996).
Aggregations of L. conchilega were shown to possess some resistance to trawling when only several
consecutive trawls resulted in a negative effect on
numbers of L. conchilega (Rabaut et al. 2008).
However, the associated fauna of the tube-worm
was shown to change significantly after a one-off
experimental trawl in the inter-tidal zone.
Generally, species associated with L. conchilega
seemed to be either vulnerable to beam trawling or
they were negatively associated with L. conchilega
under undisturbed conditions and increased in density after disturbance by beam trawling. This was
found to be true for sub-tidal areas where close
associates of L. conchilega, such as the polychaetes
Eumida sanguinea, Phyllodoce mucosa and Eteone
longa as well as some other co-occurring species
(e.g., Abra alba and Kurtiella bidentata) were
shown to be significantly impacted by trawling
(Vanaverbeke et al., 2009). Densities of opportunistic
species such as the polychaetes Capitella sp.,
Heteromastus sp. and Notomastus sp., which were
considered to be negatively associated with L. conchilega, increased significantly shortly after passage of
the beam trawl. Further, it has to be considered that
the associated fauna of L. conchilega in many subtidal areas, for example along the North Sea coast, is
most probably skewed to more resistant species given
that more sensitive ones disappeared due to intensive
fishing activities, which shifted the baseline of the
benthic community structure (Callaway et al. 2007,
Reiss 2009). This indicates that L. conchilega itself
may have some resistance to intermediate beam
trawling pressure, but that the integrity of the associated species community is more vulnerable.
Other anthropogenic activities have been found
to affect L. conchilega through increased input of
particles into the system. Sludge disposal of dredged
material in the Weser estuary, for example, caused a
strong decline in L. conchilega densities (Witt et al.
2004). The polychaete was absent from the disposal
area as was its associated macrofauna, leading
to an overall decrease in benthic diversity.
Similarly, aquaculture operations with large-scale
introductions of bivalve species, such as M. edulis,
are changing the particulate composition of the
environment through the production of pseudofaeces and alterations in the hydrodynamic regime,
R. Callaway et al.
and they have the capacity to destroy pelagic larvae
(Davenport et al. 2000, Lehane and Davenport 2002).
The development of M. edulis aquaculture along a
coast may therefore have far reaching consequences
for the renewal of intertidal L. conchilega aggregations, as well as for other macrofaunal species with
pelagic larval stages.
While L. conchilega appears to be affected by high
levels of disturbance of their sedimentary environment, it is even less resistant to a natural disturbance: low temperatures. The total demise of
L. conchilega along large stretches of the Wadden
Sea coast was the result of particularly cold winters
(Buhr 1981; Strasser and Pieloth 2001). Losses were
also reported at several locations in the UK following
the severe winter of 1962–1963 (Crisp 1964). Lanice
conchilega is obviously not able to resist this disturbance, but is able to re-colonize the lost ground.
Resilience and elasticity
The resilience of L. conchilega aggregations depends
on the ability of larval and postlarval organisms to
settle in areas where aggregations of tubes suffered
some form of disturbance and were decimated or
eradicated.
The small-scale distributional patterns of
L. conchilega did not suggest much redistribution
over time and given its sessile life style, this species
may not be prone to prolific postlarval migration.
However, in two of the three areas disturbed by
cultivation of Manila clams measurable re-colonization took place after 1 or 2 years. The results tally
with other descriptions of L. conchilega’s re-colonization strategy, which appears to start with few adults
migrating into an area (Strasser and Pieloth 2001;
Zühlke 2001). These relatively low numbers of postlarval immigrants provide a holdfast for juveniles
and initiate a period of accelerated colonization.
Also, juveniles may re-colonize an area by adhering
to hard substratum such as shells of dead bivalves,
rather than attaching to tubes of adult conspecifics
(Herlyn et al. 2008). If the environmental conditions
are favorable, juveniles simply settle directly into the
sediment (Strasser and Pieloth 2001).
The duration of recovery, i.e., the elasticity,
appears to range between 1 and 4 years (Beukema
1990; Heuers et al. 1998; Zühlke 2001). In our study,
the L. conchilega population in the area of clam cultivation did not reach densities seen at the undisturbed reference site, suggesting that the interval
between the seeding and harvesting of Manila
clams was insufficient to allow full recovery.
Stability of tube-worm aggregations
Persistence
‘‘Persistent’’ is probably the most appropriate
term to describe aggregations of L. conchilega.
Although L. conchilega may not resist disturbances
particularly well, and their numbers may be regularly
decimated by the absence of successful recruitment
or by anthropogenic and natural disturbances,
L. conchilega demonstrates remarkable stamina and
success in re-colonizing areas that provide them
with a suitable habitat (see ‘‘Resilience and elasticity’’
section).
The 35-year study in the B MSM demonstrated
that some aggregations of considerable spatial
dimension can persist over decades. The study also
suggests that areas of high density of tubes are more
persistent than are sparsely populated ones.
A persistent core area with high L. conchilega
densities was surrounded by a less-dense and lesspersistent peripheral area of the aggregation. Over
time, the development of the population resembled
a heartbeat: the space L. conchilega occupied
contracted and expanded around a persistent
core. Hertweck (1995) described very similar distributional patterns to the ones found here for the
BMSM. The L. conchilega population he mapped in
the Wadden Sea covered several square kilometers,
with high densities of up to 10,000 individuals
per square meters in central parts and less dense
fringe areas with about 100 L. conchilega per square
meters.
Given the preference of juvenile L. conchilega to
settle close to adults (Callaway 2003), dense aggregations may benefit from self-amplification. The denser
the aggregation, the higher the probability of successful rejuvenation. It has to be mentioned though
that in our small-scale study the recruitment
pattern was the reverse: the dense aggregation did
not enjoy larval settlement while the sparsely populated ones did.
Lanice conchilega: reef or not reef?
Biogenic reefs provide important services for marine
ecosystems and stable reef structures are likely to be
more effective and of greater value than are transient
ones (Holt et al. 1998; Thrush and Dayton 2002).
They are also more manageable in terms of
conservation.
Lanice conchilega does not intuitively fit the concept of a reef, even when tube densities are high and
they create a characteristic mound-and-trough topography. However, in terms of effects on the benthic
fauna aggregations of L. conchilega arguably play a
reef-like role similar to other biogenic reefs such as
247
S. alveolata. Aggregations of L. conchilega alter the
community structure of the benthic fauna and
potentially enrich biodiversity and increase abundance (Zühlke 2001; Callaway 2006; Rabaut et al.
2007; Van Hoey et al. 2008). Generally, the tube
structures provide havens that allow species inhabiting the surrounding sediments to establish localized
higher densities, with few species being exclusive
to the aggregations. This is similar to reefs of
S. alveolata in which the unique nature of the associated community is not related to the presence of
particular species but is due to the juxtaposition of
species belonging to surrounding communities
(Dubois et al. 2002). The reef-forming tube-worm
F. enigmaticus also alters the abundance of macrofaunal species present in the surroundings, which
respond to the changed conditions within the reefs
(Schwindt and Iribarne 2000).
Due to the enriched associated infauna in
L. conchilega aggregations, they are of great importance for higher trophic levels such as birds and fish
(Godet et al. 2008; Rabaut et al. 2010).
Our studies have shown that aggregations of
L. conchilega are not stable in the sense of being
constantly present with continuously high tube densities over long periods of time. On the contrary,
populations are prone to considerable fluctuation
as they are vulnerable to failure of recruitment as
well as to natural and anthropogenic disturbances.
Thus, the value of L. conchilega’s ecological service
to a region will vary with the level of disturbance a
population endures.
The stability of aggregations of L. conchilega lies in
their resilience and elasticity, i.e., they recover predictably from disturbances and have proved capable
of re-colonizing lost ground in 1 to 4 years
(Beukema 1990; Heuers et al. 1998; Zühlke 2001).
The associated fauna of L. conchilega is equally, if
not more resilient than is L. conchilega itself
(Rabaut et al. 2008). This flexible response to disturbance ensures their persistence in suitable habitats
over decades, as shown for the population in the
BMSM.
Whether or not L. conchilega is a reef-builder
cannot be answered unequivocally. In terms of its
service to biodiversity, L. conchilega can certainly be
regarded as a reef-building polychaete. The key question is whether the persistent nature of L. conchilega
aggregations, with its phases of disturbance and
recovery, satisfies the criterion of longevity. We suggest that L. conchilega-rich areas with a proven
record of decadal persistence should be regarded as
a type of reef.
248
Conclusions
Our studies showed that, on the one hand, the size
and density of L. conchilega aggregations varies considerably over time. On the other hand, L. conchilega
is resilient and has a considerable potential to
recover from disturbances. As a result, large areas
are persistently inhabited by L. conchilega over decades. Given the known importance of L. conchilega
for the biodiversity and community composition of a
habitat, it can be assumed that these persistent aggregations provide reef-like services to the area over
long periods of time. We therefore suggest reconsidering the conservation status of species such as L.
conchilega, which have a proven benefit to marine
environments, but do not unequivocally fit into the
current definition(s) of reefs. A possible solution is
the clarification of the definition of a reef and to
broaden its interpretation to include species with
records of long-lasting persistence in particular areas.
Acknowledgments
We thank the National Science Foundation (IOS0938257), The Society for Integrative and
Comparative Biology Division of Ecology and
Evolution and the Division of Invertebrate Zoology,
and the American Microscopy Society for supporting
our research. This manuscript is partly the result of a
workshop that took place in Dinard (France) in
September 2009. We thank Steven Degraer and an
anonymous reviewer for their valuable comments on
an earlier version of the manuscript.
Funding
French Marine Protected Areas Agency, the CNRS
and the French Museum of National History.
Federal Ministry for Education, Science, Research
and Technology, Germany (BMBF) for project
03F0112A.
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